A survey on ectoparasites and heamoparasites of free-range indigenous chickens of Northern Tanzania

E S Swai, M Kessy, P Sanka, S Bwanga and J E Kaaya

Veterinary Investigation Centre, PO Box 1068, Arusha, Tanzania.
ESswai@gmail.com

Abstract

A survey to identify and estimate the prevalence of ecto-parasites and haemoparasite of free-range indigenous chickens in northern areas of Tanzania was conducted between November and December 2009. Three hundred and seventy three (n=373) indigenous chickens from 88 households in 9 administrative localities of northern Tanzania were examined. Of those, 83.9% had ectoparasites infestation.

The survey recorded infestation with 1 species from the order Phthiraptera (lice), one(1) species from the order Siphonaptera (fleas), and three(3) species from the order Acarina (ticks and mites). Among the ectoparasites, the most prevalent was Echidinophaga gallinacea (71.9%) followed by Menopon spp (28.5%), Argas persicus (23.9%) and Cnemidocoptes mutans (19.6%). Mixed infestation with more than 2 ectoparasite species were detected in 305(81.7%) of the birds. Fowl ticks infestation was significantly higher in Mkinga district and off bird sleeping house was significantly associated with higher infestation rate (P<0.05). The overall prevalence of slides positive for avian aegyptianellosis was 15.3 % (95% [confidence interval], CI = 11.9-19.3). Most birds were scavenging, a management system associated with a significantly higher likelihood that birds are infected to a tick-borne pathogen Aegyptinella pullorum ([odd ratio] OR = 1.93, CI = 1.03 – 3.52). Infection prevalence varied locally with flock location; with birds located in Mkinga experiencing higher odds of infection (OR = 4.5, CI = 2.5 – 8.5) compared to other districts.

Further investigations are required to establish the significance of these findings and other diseases of free-range indigenous chickens. Moreover, integrated parasite control approaches should be initiated to address parasitism in chickens in the area under study.

Key words: Aegyptiella pullorum, ectoparasites, prevalence, risk factors, Tanzania

Introduction

Chickens (Gallus domesticus) are widely kept in Tanzania and make up the largest share in terms of numbers compared to other farm animal genetic resources (Wimmers et al 2000; Msoffe et al 2001). Chicken population is estimated to be 56 million with free-range village chickens forming the largest proportion (MoLD and F 2009). Free-range production system is characterized by low input and low output, with minimal management interventions, feed supplementation, housing and disease control (Sonaiya 1990; Kitalyi 1998; Guèye 1998;   Mwalusanya et al 2002). The system is also characterized by high mortality caused by factors such as disease, predators, and poor management and nutrition (Conroy et al 2005).

In Tanzania, chickens are raised under three different management systems; the smallholder with a flock size of less than 50 birds, semi-commercial system with flock sizes ranging from 50 to 5,000 and the commercial system where over 5,000 birds are kept. In the village extensive poultry production however, the overriding constraint to expansion and increased productivity of the scavenging chicken population is their frequent decimation by Newcastle disease (ND), predation, thefts and parasite infestations (Yongolo et al 1997; Conroy et al 2005).

Where studies have been conducted, parasitic diseases, and in particular ectoparasites and haemo-parasites have been identified as the major impediment to chicken health world wide owing to the direct and indirect losses they cause (Permin et al  2002; Sonaiya and Swan 2004; Swai et al 2007). However, ectoparasites has received less attention in almost all the production systems, and there is no or scant documentation for avian haemoparasites in Tanzania (Fallis et al 1973; Msami 2002). Studies have shown that in the extensive management systems, where the chickens have access to outdoor areas and not confined do have a greater diversity of parasites (Pandey et al 1992; Permin and Hansen 1998). These parasites are of great economic importance to poultry industry (Derylo 1974; Gless and Raun 1959, Panda and Ahluwalia 1983).The factors leading to low productivity and performance of this specie of birds is multifctorial in dimension. The limitation imposed on the productivity and performance of chicken by the infestation and infection with disease causing agents can not be overemphasized. Little research has been published on rural poultry health, despite the fact that up to 80% of the poultry population in Tanzania is kept by the households as free-range chickens (Minga et al 1989; FAO 2000).

The objective of this study was to identify and to determine the prevalence of ecto- and haemoparasites affecting free-range chickens from different administrative localities of northern Tanzania. The results can be used in making objective decisions in control strategies.

Material and methods  

Study sites

This study which forms part of a broader study on Newcastle disease (ND) and highly pathogenic avian influenza (HPAI) using participatory disease search (PDS) approach was undertaken in four regions (Tanga, Kilimanjaro, Arusha and Manyara) comprising 9 administrative localities (lat 2’11 and 6’14S, longt 35’11 and 38’26E) of northern Tanzania (Figure 1).

The climate is sub-humid with temperatures ranging from 14^oC to 23^oC on high elevation areas and 30^oC to 37^oC along north coastal Indian Ocean shore. The study areas experiences  two main seasons, the dry season, from May to October and the wet season, from November to April with rainfall ranging from 635 mm to 3,050 mm, with low rainfall in the low laying areas and high rainfall on high altitude and plateau areas.

Area/household selection and data collection

Study districts were selected on the basis of high perceived risk for HPAI occurrence; located within wild bird migratory flyways, extensive poultry trade activities and the low level of bio-security employed. Households for the study were randomly selected based on the past experience of chicken keeping, possession of chicken(s) and willingness to participate in the study. This sampling procedure resulted into 9 administrative districts and 88 households. Primary data related to chicken production were collected through consultative procedures from various sources including respective district agriculture and livestock (department) offices. The data (secondary), coupled with checklist and farm inspection was collected using semi-structured questionnaires which was completed at all the selected household on a single visit. The questionnaire was administered using the national Swahili dialect by a veterinary department staff member, who was trained in participatory research methodologies. Important household and flock-level data recorded included location, owner, source (brought in or homebred), health status at a time of visit (subjectively classified as healthy or unhealthy), sex, housing (classified as permanent chicken pen or household living house), external parasite type and infestation categorized as (binary variable; Yes or No).  Birds were categorized as follows: chicks (aged between 1- 3 months), growers (>3-9 months) and adult (aged > 9 months). The data was collected during the period of November to December 2009.

Husbandry system

The main form of poultry production is the extensive or backyard system where scavenging is the main feeding system with little or no supplementation (Smith 1992). The flocks are normally small in size but are an important asset used as a source of income for households and by providing their owners with meat and eggs that can be consumed by the family. The birds are housed at night in owner’s living house or in simple bird pen (Banda) constructed from local available materials. The breeding system used is natural mating, with service cockrels running freely with females year-round (Horst 1990). Prevention against diseases and helminthes are hardly provided. Most farmers depend on hawkers or middlemen who buy the birds for urban markets (Sonaiya 1990; Mlozi et al 2003)

Sampling and analysis

A total of 373 chickens from 88 households within 9 administrative locations of northern Tanzania were examined for ectoparasites and haemoparasites. A representative of ectoparasites found in the body of the chicken was collected in the universal bottles containing 70% alcohol and the predilection sites on the body noted. Skin scrapings of chicken with scaly lesions were collected using scalpel blades into universal bottles containing 10% potassium hydroxide. Collected samples were transported to the Entomology laboratory at the Veterinary Investigation Centre (VIC), Arusha for identification (Plates a, b, c, d).

The ticks were identified using tick identification keys available from different sources (Ruedisueli and Manship 2006; Walker et al 2003; Bowman and Lynn 1995). Other ectoparasites; fleas, mites and lice were examined with dissecting microscope and identification carried out according to guidelines described by Soulsby (1982) and Permin and Hansen (1998).

Parasitological examination

Thin blood smears were prepared from drops of blood taken from the wing vein using disposable sterile syringes (3 ml) and needles (21G 1¹/₂), air dried and fixed in the field in100% methanol within 1–2 h. They were stained for 45 min in Giemsa’s stain (diluted 1:3 in buffer, pH 7.2) on arrival in Veterinary Investigation Centre, Arusha. Each smear was examined under oil immersion at a power magnification of x100 in the objective lens and x10 in the eyepiece lens. Haemoparasites detected were identified according to the guides described by Permin and Hansen (1998).

Statistical analysis

A database was developed to store quantitative data from this cross sectional study using Epi Info version 6.04d software (CDC, Atlanta 1996). The same programme was used to compute descriptive statistics of variables collected during the study. Chi–square analysis was used to compare the association dependent (ecto-parasite infestation and heamoparasites infection) and independent variables (location, sex, age category, source, healthy status, level of ectoparasites infestation) investigated. A critical probability of 0.05 was adopted throughout as a cut-off point for statistical significance between variables compared.

Results  

Descriptive statistics

All visited villages households (n=88) were interviewed and their flock sampled and examined for ectoparasites infestation. A voluntary participating rate of 100 % was therefore achieved. Five species of ectoparasites were identified to be common and their respective infestation prevalence and predilection sites are given in Table 1.

Analysis of the prevalence of ectoparasites on birds

One species of chewing lice (genera: Mallophaga), one species of fleas (genera: Siphonaptera) and three species of mite and tick (genera: Acari) were detected from 373 examined birds in this study.  The mites included Cnemidocoptes mutans and Dermanyssus gallinae. The lice were Menopon spp. The flea was Echidnophaga gallinacea and the tick was Argas persicus. Overall prevalence of ectoparasites infestation was 83.9%. Overall, fleas had the highest frequency of occurrence, with a 75.3% prevalence closely followed by the chewing lice, Menopon spp with a prevalence of 28.5%.  Other identified ectoparasites and their frequencies included Argas persicus, 23.9% and Cnemidocoptes mutans/ Dermanyssus gallinae 19.6 % (Table 1). Mixed infestations were also observed. Mixed infestation with two ectoparasites fleas and lice were detected in 91(24.4%) of the sample, while 305(81.7%) of the birds were infested with more than 2 ectoparasites species. The prevalence of tick infestation was mostly affected by housing and geographical location of the birds. Birds located in Mkinga districts and the one living in non-bird house were more likely to carry Argas persicus tick ([odd ratio], OR = 2.2 for Mkinga and 3.24 for human living house; P<005 for both) compared to other localities. The odds that birds carried an adult Echidnophaga gallinacea did vary amongst administrative regions when subdivided by district with the odds being significantly higher in the Maramba sub-district than the Mkinga district (90% vs. 37%: p< 0.05).

Prevalence and factors associated with Aegyptiella pullorum infection

The most parsimonious univariable model is presented in Table 2. Aegyptiella pullorum was detected in 57(15.3%, 95% [confidence interval], CI = 11.8-19.3) in samples analysed and there was no any other heamoparasites detected in the samples. Significant factors associated with prevalence of Aegyptiella pullorum included bird administrative location and the level of tick infestation. In a univariable analysis, birds that carried one or more Argas persicus ticks were significantly more likely to be infected by Aegyptiella pullorum (OR = 1.93, CI = 1.03 – 3.52, P = 0.032). Birds located in Mkinga district were significantly more likely to be infected by Aegyptiella pullorum compared to other localities (OR = 4.5, CI = 2.5 – 8.5, P<0.001). None of the other investigated flock and bird level factors were associated with differences in prevalence values. 

Discussion 

In this study, there was evidence that infestation of birds to various species of ectoparasites was widespread in the study regions. Furthermore, there was evidence of geographical variation in the exposure and distribution of blood parasite Aegyptiella pullorum amongst the nine administrative localities. From the results obtained from this study, ‘sticktight’ flea was the commonest ectoparasites found in free-range village chickens in these regions which are in agreement with the work done in Tanzania previously (Msami 2002). However, in a similar work done earlier by Permin et al (2002), Cnemidocoptes mutans, Dermanyssus gallinae and/or Echidnophaga gallinacea were encountered more often than other ectoparasites. The type of management might have contributed to the difference observed in the type of ectoparasites that predominated. Arend (1997); noted that management influence the parasites that are predominant in poultry flock.

Occurrence of Echidinophaga gallinacea and Argas persicus was significantly (p<0.001) affected by administrative location, with prevalence being consistently higher in adult birds and in Mkinga (subdivision Maramba) as compared to other districts. The explanation for this is yet to be found. The eco-climate attributes of Maramba i.e. wet, humid weather which permit high densities and varieties of vectors of medical importance, may similarly promote high densities of Argas persicus which is the potential vector of Aegyptiella pullorum (James 1979).

In the present study, 84% of the chickens from the free-range production system harboured ectoparasites at varied level and species. This is comparable to a recent study in Nigeria and Zimbabwe, which reported high prevalences of ectoparasites in domestic free-range chickens and included all the species found in this study (Okaeme 1988; Permin et al 2002). Consistent to other studies in the tropics, the free-range system strongly favoured occurrence of all the parasites (Abebe et al 1997; Permin et al 2002). This clearly indicates that the parasites infect the chickens either through contact with other infected chickens or from the environment as they scavenge together in this system. Some of the importance of most ectoparasites transcends the direct impact on poultry production. Apart from irritations, depression uneasiness and annoyance they cause on birds, they are vectors of some poultry diseases and they directly limits the protein available to man through lowered productivity and mortalities. Some of these parasites encountered in this study are noted either to infest man or cause annoyance especially in rural settings where there is close association between man and domestic fowls.

Aegyptiella pullorum was the single prevalent haemoparasite found in this study. It is considered to be highly pathogenic to chickens with mortality risks in the range of 30-80% amongst young birds (Soulsby 1982). Presence of Aegyptiella pullorum which is believed to cause anaemia, lowered growth and production, emaciation, diarrhoea, fever and paralysis in chickens (Levine 1985; Permin and Hansen 1998; Mays and Aiello 1998) may be an indicator of presence of Argas persicus which is a vector for this blood parasite.  Affected birds appeared ruffle with poor appetite and diarrhea (Permin and Hansen 1998). Argas persicus is known to infest man especially children (Arend 1997). There are no reports on A.pullorum prevalence in Tanzania with which to compare the results of this study (Fallis et al 1973). However, data from a study in West and Southern Africa and other environments similar to Tanzania indicate that Aegyptiella pullorum infection can be quite widespread among free range birds raised in the tropics. For example, in the blood smear Giemsa-based investigations, prevelences of 9% and 6% have been reported in Ghana, and Zimbabwe, respectively (Kelly et al 1998; Poulsen et al 2000; Permin et al 2002).  The detected prevalence of infection in the birds was generally higher than those observed in West and Horn of Africa where Aegyptianellosis is also considerd a major health important disease to free-range chicken production (Ashford et al 1976). The variability in the prevalence of Aegyptiella pullorum between reports could be attributed to difference in management system of the birds, eco-climates or levels of infestation of Argas persicus in the area.

Conclusions

• The prevalence of ectoparasites infestation was high in the study regions, mostly likely due to free scavenging poultry managements, but Aegyptiella pullorum is common and is widely distributed in the study regions. Birds were more likely to be infected by Aegyptiella pullorum if they had history of contacts with ticks and ecto-parasite infestation varied considerably with geographical location at a varying scale.

  
  

• Based on these results, it is clear that avian ecto-and haemoparasites are present in Tanzania, some of which are reported to be of great health and economic importance in literature. Practically, results from this study will be used in development of extension messages for the farmers regarding the best husbandry procedures to adopt and time to apply control interventions.

Acknowledgements

The authors are very grateful to the flock owners, field staff who gave their time to this research. In addition, thanks are due to the staff of VIC for their cooperation and technical assistance. We also thank the Director, Directorate of Veterinary Services, for permission to publish this work.

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Received 4 May 2010; Accepted 2 August 2010; Published 1 September 2010

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